Afterhyperpolarization (AHP) regulates the frequency and timing of action potentials in the mitral cells of the olfactory bulb: role of olfactory experience

Abstract

Afterhyperpolarization (AHP) is a principal feedback mechanism in the control of the frequency and patterning of neuronal firing. In principal projection neurons of the olfactory bulb, the mitral cells (MCs), the AHP is produced by three separate components: classical potassium-mediated hyperpolarization, and the excitatory and inhibitory components, which are generated by the recurrent dendrodendritic synaptic transmission. Precise spike timing is involved in olfactory coding and learning, as well as in the appearance of population oscillatory activity. However, the contribution of the AHP and its components to these processes remains unknown. In this study, we demonstrate that the AHP is developed with the MC firing frequency and is dominated by the potassium component. We also show that recurrent synaptic transmission significantly modifies MC AHP and that the strength of the hyperpolarization produced by the AHP in the few milliseconds preceding the action potential (AP) emission determines MC firing frequency and AP timing. Moreover, we show that the AHP area is larger in younger animals, possibly owing to increased Ca2+ influx during MC firing. Finally, we show that olfactory experience selectively reduces the early component of the MC AHP (under 25 msec), thus producing a modification of the AP timing limited to the higher firing frequency. On the basis of these results, we propose that the AHP, and its susceptibility to be selectively modulated by the recurrent synaptic transmission and olfactory experience, participate in odor coding and learning by modifying the frequency and pattern of MC firing.

Opto nongenetics inhibition of neuronal firing

“…On the other hand the modification of AP shape with changing temperature has been ascribed to an increase in amplitude, duration, and steepness of voltage dependent potassium currents and to an increase in amplitude but a decrease in the width of voltage‐dependent sodium currents (Volgushev, Vidyasagar, Chistiakova, Yousef, et al., ). Similar mechanisms could explain the effect of light on the AP shape in MCs, as well as the observed increase in the fast AHP, mainly due to the activation of voltage‐dependent potassium channels in these neurons (Duménieu et al., ).…”

“…This latter hypothesis is in line with the reported reduction in membrane resistance produced by a temperature increase (Thompson et al., ; Volgushev, Vidyasagar, Chistiakova, Yousef, et al., ). The increase in AP latency and AHP amplitude would also promote a reduction in firing in MCs (Duménieu et al., ). Finally, the apparent reduction in glutamatergic transmission and in particular the recurrent synaptic excitation, will also lead to a reduction in MC firing (Salin, Lledo, Vincent, & Charpak, ).…”

“…Light effect on AP will be assessed by generating a single action potential by a 5 ms positive current injection both in the absence (NO LED) and presence (LED) of light. Two AP parameters will be evaluated: AP amplitude, calculated as the difference between AP peak and the average V m in the 100 ms that precedes the current step, and AP latency, calculated as the time between the beginning of the current step and AP peak (Duménieu, Fourcaud‐Trocmé, Garcia, & Kuczewski, ). Statistical effect will be assessed by paired bilateral test.…”

Characterization of Functional Effects of Two New Active Fractions Isolated From Scorpion Venom on Neuronal Ca2+ Spikes: A Possible Action on Ca2+-Dependent Dependent K+ Channels

“…There are also other reports indicating that exposure to scorpion venom peptides cause the enhancement of neuronal excitability by suppressing the AHP (Ishii et al, 1997; Juhng et al, 1999; Pedarzani et al, 2002). In many neurons, Ca 2+ entry through activation of Ca 2+ leads to opening the Ca 2+ dependent potassium channels and thereby regulates cell excitability (Lancaster, Adams, 1986; Sah & Faber., 2002; Janahmadi et al, 2008; Duménie, Fourcaud-Trocmé, Garcia, & Kuczewski, 2015). In the present study, in common with KTX the two new active scorpion toxin fractions enhanced firing frequency by reducing the amplitude of AHP (Haghdoost-Yazdi, Janahmadi, & Behzadi, 2008).…”

Tune it in: mechanisms and computational significance of neuron-autonomous plasticity

“…Learning-induced modification of each of these components creates a different time-variant and frequency filtering, and therefore modulation of each of the currents enables a finetuning of the spike pattern (Faber and Sah 2003;Pozzorini et al 2013;Sah 1996). Modulation of the fast AHP currents will affect the high-frequency regime at the beginning of the burst (Duménieu et al 2015), and modulation of the slow AHP currents will be more affective in the low-frequency regime at the end of the synaptic burst (Faber and Sah 2005;Guan et al 2013).…”